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INVITED REVIEW
Orchid pollination: from Darwin to the present day
CLAIRE MICHENEAU1*, STEVEN D. JOHNSON2 and MICHAEL F. FAY
boj_995
1..19
FLS3
1
UMR 53 Peuplements Végétaux et Bio-Agresseurs en Milieu Tropical, Université de La Réunion, 15
avenue René Cassin BP 7151, 97715 Saint-Denis Messag Cedex 9, La Réunion, France
2
School of Biological and Conservation Sciences, University of KwaZulu-Natal, P Bag X01,
Scottsville, Pietermaritzburg 3209, South Africa
3
Jodrell Laboratory, Royal Botanic Gardens, Kew, Surrey TW9 3AB, Richmond, UK
Received 22 April 2009; accepted for publication 3 August 2009
In this year celebrating the bicentenary of the birth of Darwin and the sesquicentennial of the publication of
Darwin’s On the Origin of Species, the present paper aims to assess the impact of Darwin’s legacy on the history
of orchid pollination biology. To illustrate the major contribution of Darwin to this fascinating biological field, we
focus on the large angraecoid orchid group and propose an overview of the complex relationships that these orchids
have developed with specific pollinators. We further discuss how Darwin’s seminal work on the angraecoid orchid
Angraecum sesquipedale triggered the beginning of a long debate about the evolution of long floral spurs and why
his idea of reciprocal evolution or ‘coevolution’ was one of the great contributions to evolutionary biology. © 2009
The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 1–19.
ADDITIONAL KEYWORDS: angraecoid orchids – bird pollination – hawkmoth pollination – long spur –
Madagascar – Mascarene Islands – Orchidaceae.
INTRODUCTION
For the celebration of the bicentenary of Charles
Darwin’s birth and the sesquicentennial of the publication of his On the Origin of Species (Darwin,
1859), the world is re-exploring the impact of Darwin
and his theory of evolution on science and society.
However, it is not possible to commemorate Darwin’s
legacy without consideration of orchids, which took a
central place in his main achievements, and to which
he devoted many years of study: ‘I never was more
interested in my life in any subject than this of
orchids’ (Darwin, 1861 in a letter addressed to
Hooker).
The subject of the present paper is to revisit the
history of orchid pollination biology from the time of
Darwin to the present day, with an emphasis on the
*Corresponding author.
E-mail: [email protected]
pollination mechanisms involved in the angraecoid
orchids, including the famous long-spurred Madagascan species, which, through Darwin’s meticulous
observations and innovative reasoning, served to
bring the orchid family into the heart of evolutionary
research on plant–pollinator interactions.
ORCHID POLLINATION: A BRIEF HISTORY
FROM DARWIN’S TIME TO THE 1930S
Although, by the end of the 18th century, earlier
botanists including Bernard de Jussieu and Michel
Adanson had contributed to the better understanding
of the general structure of orchid flowers, pollination
mechanisms in orchids were first fully detailed by
Darwin in his famous book, On the various contrivances by which British and foreign orchids are fertilised by insects and the good effects of intercrossing
(Darwin, 1862). In addition to being ‘an inspiration to
floral ecologists of his and later time’ (van der Pijl &
Dodson, 1966), Darwin’s book remains a classic today.
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 1–19
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C. MICHENEAU ET AL.
In this book, he described his own observations on
the pollination of many British orchids, his personal
interpretations of the pollination mechanisms
involved in some tropical species, mainly based on
floral morphology, and his views on homologies in
orchid flowers. The second edition, published in 1877,
included an extended part dedicated to tropical
orchids, based mainly on the observations made by
his contemporary Fritz Müller (Darwin, 1877). These
two books, in which Darwin clearly demonstrated
that orchids provide strong evidence for natural
selection and for adaptations that promote crosspollination, were written partly in support of his
theory of evolution, which invoked much criticism
after the publication of On the Origin of Species in
1859 (Darwin, 1859). However, Darwin’s idea that
orchids provide evidence for adaptations to insect
pollination found strong support among naturalists
and influenced as never before the future directions of
the fascinating field of orchid pollination biology.
From that time until the 1920s, the Western world
raced to gather information on insect–flower interactions, involving ‘most of our knowledge on the pollination mechanisms and insect visitors of European
and North American flowers’ (Proctor, Yeo & Lack,
1996).
The next major contribution to orchid pollination
had to wait for the end of this descriptive period and
the discovery of pseudocopulation in the genus
Ophrys L. in Algeria (Correvon & Pouyanne, 1916;
Pouyanne, 1917) and, soon after, in the genus Cryptostylis R.Br. in south-eastern Australia (Coleman,
1927). Sexual deception in flowers which mimic the
signals of female insects, in some cases so accurately
that they elicit copulatory behaviour in male insects
(pseudocopulation), is almost exclusive to orchids and
constitutes one of the most fascinating pollination
mechanisms found in the family, if not in all flowering
plants. Male insects are sexually attracted to the
flower by a floral scent that imitates the olfactory cue
or sex pheromone(s) of the female, often enhanced
with a resemblance to the female in shape, colour and
texture, and usually pick up and deposit pollen while
they attempt copulation with flowers. Since its discovery in the 1920s, sexual deception has been found
in a number of other orchids and remains an active
topic of interest in orchid pollination and evolution
(e.g. Schiestl et al., 1999, 2003; Ayasse et al., 2002;
Singer, 2002; Singer et al., 2004).
FROM
THE
1930S
TO THE
1960S
During the next three decades, interest in orchid
floral biology and pollinator observations declined, as
the attention of biologists shifted to new disciplines
such as cytology and genetics. It was only in 1966
that the second classic book of orchid pollination,
Orchid flowers, their pollination and evolution, was
published to commemorate the centenary of the publication of Darwin’s book (van der Pijl & Dodson,
1966). In addition to being a review of one century of
orchid–pollinator observations, this book constituted
a major update, taking advantage of recent observations by the authors themselves and contributions
provided by other famous orchidologists including
R. L. Dressler and B. Kullenberg. Van der Pijl and
Dodson presented a modern appreciation of orchid
pollination syndromes with an emphasis of the major
role played by pollinators in the evolutionary history
of the orchid family. In this, their views were deeply
rooted in Darwinian thought.
SINCE
THE
1960S
From the end of the 1960s, there was a resurgence of
interest in pollination studies. This can be attributed
to the development of ecology and new evolutionary
concepts and models, many of which were integrated
into the field known at that time as ‘biosystematics’
(Proctor et al. 1996). In addition, the formalization of
new principles and methods (Jones & Little, 1983;
Willson, 1983; Dafni, 1992; Kearns & Inouye, 1993)
contributed to a redefinition of the scope of pollination
studies as an integrated part of broader studies of
reproductive biology and population dynamics. Especially in orchids, in which pollinator activity could be
easily quantified by pollinarium removal and deposition, an incredible volume of quantitative data on
pollination and reproductive success, both in time and
space, has been gathered throughout the world: in
Europe and North America (e.g. Nilsson, 1981, 1983a;
Gigord, Macnair & Smithson, 2001; Smithson &
Gigord, 2001; Smithson, 2002), the Neotropics and
Australia (e.g. Romero & Nelson, 1986; Peakall,
Beattie & James, 1987; Peakall, 1989; Zimmerman &
Aide, 1989; Ackerman & Montalvo, 1990; RodríguezRobles, Meléndez & Ackerman, 1992; Ackerman,
Rodríguez-Robles & Meléndez, 1994; Ackerman,
Melendez-Ackerman & Salguero-Faria, 1997; Tremblay et al., 1998; Borba & Semir, 1999; Borba, Shepherd & Semir, 1999; Salguero-Faría & Ackerman,
1999; Singer & Cocucci, 1999; Parra-Tabla et al.,
2000; Borba & Semir, 2001; Singer, 2001; Borba et al.,
2002; Singer, 2002; Schiestl et al., 2003; Singer et al.,
2004) and in South Africa (Steiner, Withehead &
Johnson, 1994; Johnson & Steiner, 1997; Johnson,
1997a, b; Johnson & Kurzweil, 1998; Johnson, Linder
& Steiner, 1998; Ellis & Johnson, 1999). Although
noteworthy books and reviews contributed to enhancing our knowledge of the identity and specificity of
orchid pollinators and their role in orchid evolution
(e.g. Ackerman, 1986; Nilsson, 1992; Tremblay, 1992;
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 1–19
ORCHID POLLINATION
van der Cingel, 1995; Johnson & Steiner, 2000; van
der Cingel, 2001; see also Dressler, 1993), three publications, in particular, have synthesized the main
conclusions that arose from this productive period.
Firstly, Neiland and Wilcock (1998) undertook a comparative study of the reproductive success among 117
nectariferous and nectarless orchids, from both
temperate and tropical regions. They confirmed the
hypothesis that nectariferous orchids are more successful in setting fruit than nectarless species, but
they also expressed concern about the lack of data on
reproductive success in the tropical regions. Secondly,
Tremblay et al. (2005) presented an extensive overview of orchid floral biology and reproductive success
and their evolutionary consequences for orchid diversification. They reaffirmed that the seed production in
representatives of the family is frequently strongly
pollinator-limited and suggested that genetic drift,
related to the small number of individuals that participate in reproduction when there is pollen limitation, could have played a role in the extraordinary
diversification of the family. Thirdly, Jersáková,
Johnson & Kindlmann (2006) reviewed the mechanisms of deceptive pollination in the orchid family
and the various hypotheses that have been put
forward to account for their evolution. They concluded
that promotion of cross-pollination was the most compelling argument for the evolutionary maintenance of
floral deception in about 40% of species in the family.
In addition, the combined development of molecular
biology (DNA sequencing) and phylogenetic methods
during the last two decades opened a vast new field of
investigation, allowing the scientific community to
revisit hypotheses about relationships among organisms. The mapping of pollination syndromes (or
pollinator-linked floral traits) onto phylogenetic trees
has provided new insights into the ecological determination of evolutionary transitions, their polarity,
the extent to which changes were evolutionarily labile
or constrained and the extent to which radiations can
be explained by key trait innovations (e.g. Larsen
et al., 2008). A comprehensive phylogeny of the orchid
family based on molecular data was lacking until the
contribution of Chase et al. (2003) and such phylogenies have been crucial in determining evolutionary
transitions, especially for orchids in which extensive
floral convergence as a result of pollinator-mediated
selection has occurred.
Recently, Ramírez et al. (2007) estimated ages for
the origin of the orchid family and each subfamily
based on pollinia found fossilized in amber. We can
now explore how orchid–pollinator interactions developed over time, which may allow us to distinguish
between coevolution (plants and pollinators evolve
together reciprocally) vs. sequential evolution (when
the evolution of one group follows another).
3
Pollination remains an active field of research and
papers are still being published in large numbers as
new data are accumulated. Some groups of orchids
have been and still are the focus of study, including
various members of the largest subfamily, Epidendroideae (e.g. Stpiczyńska, Davies & Gregg, 2007;
Brys, Jacquemyn & Hermy, 2008; Chase et al., 2009;
Pansarin, de Moraes Castro & Sazima, 2009), the bee
orchids and their allies (Ophrys L., Orchidoideae, e.g.
Cortis et al., 2009; Devey et al., 2009; Schlüter et al.,
2009) and the lady’s slipper orchids (species of Cypripedium L., Cypripedioideae, e.g. Bänziger, Sun &
Luo, 2008; Case & Bradford, 2009; Li et al., 2008), for
which an elegant new method for studying pollination
was recently published by Case & Bradford (2009). In
a recent special issue of Annals of Botany focusing on
orchid biology (Fay & Chase, 2009, and associated
papers), pollination of orchids was discussed in
several papers. In addition to two reporting pollination studies (Cheng et al., 2009; Peter & Johnson,
2009), these discussed pollination in relation to taxonomy and phylogenetic relationships (Chase et al.,
2009; Hopper, 2009; Salazar et al., 2009; van den Berg
et al., 2009), species delimitation (Cortis et al., 2009;
Devey et al., 2009; Hedrén & Nordström, 2009),
inbreeding vs. outbreeding (Duffy et al., 2009); invasiveness (Cohen & Ackerman, 2009), conservation
(Swarts & Dixon, 2009) and evolutionary development (Mondragón-Palomino & Theißen, 2009).
CASE STUDY: ANGRAECOID ORCHID
POLLINATION
BACKGROUND
The angraecoid orchids (Epidendroideae Lindl.,
Vandeae Lindl., Angraecinae Summerh. sensu lato;
see below) are a large group of monopodial epiphytic
orchids, including more than 760 species. Two genera
have diversified in Central and South America and
the Caribbean (Campylocentrum Benth. and Dendrophylax Rchb.f.), but most of these orchids are the
product of an extensive radiation in the western
Indian Ocean, including Africa, Madagascar and
nearby islands. Although angraecoid orchids were historically referred to two subtribes, Angraecinae (c. 17
genera, 410 species, mostly from Madagascar) and
Aerangidinae Summerh. (c. 32 genera, 350 species,
mostly from Africa) (e.g. Schlechter, 1926; Dressler,
1981, 1993; Chase et al., 2003), recent insights from
molecular data provided evidence to support recognition of a single subtribe, Angraecinae, which includes
all angraecoid orchids (i.e. Angraecinae sensu lato;
Carlsward et al., 2006).
The Old World angraecoid orchids are known for
their white, spectacularly long-spurred flowers highly
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 1–19
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C. MICHENEAU ET AL.
specialized for hawkmoth (sphingid) pollination. The
study of the pollination biology of these orchids
started with the famous prediction by Darwin, which,
in spite of being widely known, deserves to be
repeated here. Darwin received some specimens of
Angraecum sesquipedale Thou. and was particularly
intrigued by the peculiar flowers of this strange
orchid which, for the plants he examined, had a
nectar tube approximately ‘11 and a half inches long’
(almost 30 cm). After meticulous floral observations
and different experiments of manual pollination, he
concluded that only a giant hawkmoth with a ‘wonderfully long proboscis’ would be able to pollinate this
spectacular orchid. The predicted pollinator, Xanthopan morganii var. praedicta, was found 41 years later
in the primary forests of Madagascar (Rothschild &
Jordan, 1903), but effective pollination of the orchid
by this animal was only demonstrated 135 years after
Darwin’s prediction (Wasserthal, 1997)! In addition
to predicting the existence of a giant hawkmoth on
Madagascar, Darwin suggested that the extraordinary length of the spur of A. sesquipedale was driven
by natural selection because of an advantage for
reproduction success when the spur is longer than the
moth proboscis and the head of the moth presses
firmly against the orchid column, enhancing pollination. Conversely, if the orchid spur was longer than
the proboscis, selection would favour a longer proboscis because this would enable the moth to gain access
to more nectar. Darwin thus posited that there would
be a kind of arms race between the spur length of the
orchid and the proboscis of the moth (see Nilsson,
1988; Anderson & Johnson, 2008; Pauw, Stofberg &
Waterman, 2009). This idea of reciprocal evolution or
‘coevolution’ was one of Darwin’s great contributions
to evolutionary biology.
Since this famous prediction, the large genus
Angraecum Bory has received much attention from
evolutionary biologists (e.g. Wallace, 1867, 1871;
Nilsson, 1992, 1998b; Wasserthal, 1997). However,
floral morphology is diverse within the genus, and in
the subtribe, suggesting variation in pollination
systems. Notably on the Mascarene islands (Mauritius, Reunion and Rodriguez, Indian Ocean), three
species (Angraecum striatum Thou., A. bracteosum
Balf.f. & S.Moore and A. cadetii Bosser) are particularly interesting because their white flowers have
short, wide spurs. These features were sufficiently
uncommon in the genus to prompt Bosser (1987) to
revise section Hadrangis Schltr. to include only these
three species, making the section endemic to the
Mascarenes. Pollinator observations have shown that
two of these species are pollinated by small songbirds
from the family Zosteropidae (white-eyes) on Reunion
(Micheneau, Fournel & Pailler, 2006; Micheneau
et al., 2008c), whereas the third species, A. cadetii
(Reunion and Mauritius) has a highly surprising pollinator, a raspy cricket (Gryllacrididae from the order
Orthoptera) (Micheneau et al., in press). At the opposite end of the scale, all endemic long-spurred species
are self-pollinated on Reunion (Micheneau, 2005;
Micheneau et al., 2008b; see also Jacquemyn et al.,
2005). These evolutionary shifts (from outcrossing to
selfing and between different pollinators) are related
to recent dispersal to the Mascarene Islands, where
specific long-tongue pollinators of ancestral orchid
colonists were probably absent. From combined phylogenetic, biogeographic and ecological data, it now
appears that angraecoid orchid diversification was
strongly associated with interactions with the pollinator fauna on Reunion (Micheneau et al., 2008a). In
contrast, self-pollinating species appear less likely to
be involved in adaptive radiations. In the following,
we survey the current state of knowledge of the
pollination of angraecoid orchids.
METHODS
INVOLVED IN POLLINATOR OBSERVATION
Various methods have been used to observe pollinators foraging on angraecoid orchid flowers and these
are representative of methods that may be used to
observe pollinator activity on plants more generally
(see also Kearns & Inouye, 1993). Pollinators may be
identified directly in the field by observing their foraging on flowers. Direct observations are commonly
undertaken in a time period that corresponds to the
main activity of the expected pollinators (i.e. the
evening in the case of hawkmoth pollinators, e.g.
Martins & Johnson, 2007). However direct observations may be time-consuming, particularly if there are
low visitation rates or if pollinator behaviour is
altered by human presence (e.g. birds). Depending on
the behaviour of pollinators, direct observations may
also involve difficulties in distinguishing simple visitors from efficient pollinators. Videotape observations
in the field offer a good alternative for observing
pollinator visits without influencing their behaviour
and without spending days in front of flowers while
nothing is happening. The development of hard-disk
camcorders with night option, combined with the use
of long-duration rechargeable batteries and a waterproof casing, now allow the observation of pollinators
for more than 12 h, whatever the time of day or night
and whatever the weather (Micheneau et al., 2006,
2008c, in press). It is also possible to identify pollinators using indirect techniques: identifiable pollinaria may be found on pollinators caught on flowers
of non-orchid species or at a light trap (e.g. Dressler,
1981; Nilsson et al., 1985, 1987; Luyt & Johnson,
2001) and identifiable insect scales and hairs may
be found on orchid stigmas (e.g. Nilsson & Rabakonandrianina, 1988). In these cases, pollination
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 1–19
ORCHID POLLINATION
mechanisms can be deduced on the basis of floral
morphology and the attachment of pollinaria on the
body of the pollinators, even if observations have been
largely unsuccessful in the field (e.g. Nilsson & Rabakonandrianina, 1988; Luyt & Johnson, 2001).
BREEDING
SYSTEMS
All angraecoid orchids that have been studied are
self-compatible (Nilsson & Rabakonandrianina, 1988;
Luyt & Johnson, 2001; Micheneau, 2005; Micheneau
et al., 2006, 2008b,c; Martins & Johnson, 2007; see also
Dressler, 1993). In almost all cases, fruit set is not
significantly different between self- and crosspollinated flowers. However, in Mystacidium venosum
Harv. ex Rolfe, self-pollination significantly decreased
fruit weight, fruit length and the percentage of seeds
with embryos, which could reflect either partial selfincompatibility or, more likely, strong inbreeding
depression (Luyt & Johnson, 2001). These patterns
are like those observed at the family level: selfcompatibility, as a result of the capacity to set fruits
from self-pollen is largely dominant within Orchidaceae (self-incompatible is estimated to occur in at
least 10% of all species; Dressler, 1993), resulting in no
difference in the number of fruits between selfed and
crossed treatments (Tremblay et al., 2005). However,
self-pollination, via a significant decrease in embryo
formation in mature capsules, tends to affect seed
production (see Darwin, 1875; Tremblay et al., 2005).
True self-incompatibility is known from just a few
orchids. Darwin stated in the second edition of The
variation of animals and plants under domestication
(1875): ‘As these orchids had been grown under
unnatural conditions in hot-houses, I concluded that
their self-sterility was due to this cause. But Fritz
Müller informs me that at Desterro, in Brazil, he
fertilised above one hundred flowers of the abovementioned Oncidium flexuosum Lodd., which is there
endemic, with its own pollen and with that taken from
distinct plants: all the former were sterile, whilst those
fertilised by pollen from any other plant of the same
species were fertile’. [For a discussion of this and other
examples of the extensive correspondence between
Darwin and Müller, see West (2003)]. According to
Tremblay et al. (2005), ‘Given the apparent costs of
self-pollination in most orchids, mechanisms that
promote outcrossing are to be expected. What is
unusual is that in orchids these are often structural
(movement of rostellum, movement of column, stigmatic maturity) and not the result of genetic selfincompatibility, dichogamy, or unisexuality (although
examples of all of these mechanisms exist in orchids)’,
which led them to address an open question for future
research: ‘is it the very existence of pollinaria and
column that has promoted the reliance of orchids on
structural mechanisms that promote outcrossing?’
5
Although all angraecoid orchids studied so far are
self-compatible, most, but not all, require pollinator
services to achieve reproduction. A notable exception
to this general rule is found on the Mascarenes,
where the six long-spurred species endemic to the
archipelago are all able to set fruit without pollen
vectors (Jacquemyn et al., 2005; Micheneau, 2005;
Micheneau et al., 2008b). Self-pollination was not
expected within the angraecoid orchids, which, as
mentioned before, have long been considered as a
highly moth-pollinator-dependent group. Within the
tribe, Dressler (1993) estimated the number of selfpollinating vandoid species as < 1%, whereas estimates of self-pollination in Orchidaceae as a whole
range between 5 and 20% of species (Catling, 1990).
However, high rates of self-pollination are not surprising in island floras; shifts to self-pollination are
thought to provide reproductive assurance when the
pollinator fauna is lacking, sparse or unspecialized
(Ackerman, 1985; Barrett, 1985; Catling, 1990;
Barrett, 1996; Eckert, Samis & Dart, 2006). On the
isolated volcanic island of Reunion, the proportion of
self-pollinating orchids is however, among the highest
in the world, estimated at 46% of species (i.e. 56 out
of 121 species of orchids; Jacquemyn et al., 2005). To
date, only the boreal flora of the northern hemisphere
has been reported to include a greater proportion of
self-pollinated species (c. 50% of c. 40 species; Catling,
1990). On Reunion, the distribution of self-pollinating
orchids is significantly correlated with the high elevational gradient found on the island (c. 2500 m; Jacquemyn et al., 2005). However, angraecoid orchids
do not follow this pattern; self-pollination in these
species is strongly positively correlated with spur
length (Fig. 1), suggesting that species specialized for
pollination by long-tongued hawkmoths underwent
selection for self-pollination because these moths
were absent or scarce at the time of colonization.
POLLINATOR
IDENTITY AND SPECIFICITY WITHIN
THE ANGRAECOID ORCHIDS
Pollinator identity
A list of published pollinators of angraecoid orchid
species is shown in Table 1. These records include
long-tongued sphingids from Madagascar and Africa,
white-eye species from the Mascarenes and insular
orthopterans (see also Fig. 2). As expected, the two
famous orchid species with the longest spurs (often
> 30 cm in length), Angraecum sesquipedale and A.
sororium Schltr., are pollinated by the two sphingid
species that possess the longest tongues in Madagascar (often > 20 cm), Xanthopan morganii var. praedicta
and Coelonia solani, respectively (Wasserthal, 1997;
Table 1). However, although the hawkmoth fauna of
Madagascar (c. 60 species) is highly endemic and
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 1–19
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C. MICHENEAU ET AL.
Figure 1. Distribution of self-pollinated angraecoid orchids on Reunion according to (A) altitude and (B) spur length
(data from Jacquemyn et al., 2005; Micheneau, 2005).
Table 1. Checklist of published pollinators of angraecoid orchids with the place of the attachment of pollinaria on the
body of the pollinator (S, sphingids; B, birds; O, orthopterans)
Orchid species
Attachment of pollinarium
Spur length > 20 cm (Madagascar)
Angraecum sesquipedale†
Xanthopan morganii (S)
Angraecum sororium†
Coelonia solani (S)
Base of the proboscis
Base of the proboscis
Spur length < 20 and > 10 cm (Madagascar, Kenya)
Angraecum arachnites*§
Panogena lingens (S)
Angraecum compactum†§
Xanthopan morganii, Panogena lingens (S)
Aerangis ellisii‡
Agrius convolvuli, Panogena lingens (S)
Neobathiea grandidierana§
Panogena lingens (S)
Jumellea teretifolia§
Panogena lingens (S)
Aerangis fuscata§
Panogena lingens (S)
Rangaeris amaniensis¶
Agrius convolvuli (S)
Aerangis brachycarpa¶
Agrius convolvuli, Coelonia fulvinotata (S)
Aerangis thomsonii¶
Coelonia fulvinotata (S)
Base of the proboscis ventrally
Base of the proboscis dorsally
N/A¶¶
Base of the proboscis dorsallly
Base of the proboscis dorsallly
Frons or palps of the head
Head or base of the proboscis¶¶
Base at the proboscis dorsally
Head or base of the proboscis***
Spur length c. 5 cm (Kenya, South Africa)
Mystacidium venosum**
Nephele accentifera aceentifera (S)
Aerangis confusa¶
Hippotion celerio, Daphnis nerii (S)
Base of the proboscis dorsally
Base of the proboscis dorsally
Spur length < 2 cm (Reunion)
Angraecum striatum††
Angraecum bracteosum‡‡
Angraecum cadetii§§
Base of the beak
Tip of the beak
Top of the head
Zosterops borbonicus (B)
Zosterops olivaceus, Z. borbonicus (rare) (B)
Glomeremus sp. (O)
*Nilsson et al. (1985).
†Wasserthal (1997).
‡Nilsson & Rabakonandrianina (1988).
§Nilsson et al. (1987).
¶Martins & Johnson (2007).
**Luyt & Johnson (2001).
††Micheneau et al. (2006).
‡‡Micheneau et al. (2008c).
§§Micheneau et al. (in press).
¶¶Pollinators were identified from hairs found on orchid stigmas.
***Not clearly precised by the authors.
N/A: Not applicable.
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 1–19
Figure 2. Illustrations of different pollinator groups. A, Hippotion celerio visiting flowers of Mystacidium capense (L.f.) Schltr. (South Africa, picture from S. D.
Johnson). B, C, Angraecum striatum and its bird-pollinator Zosterops borbonicus (grey white-eyes) with pollinaria attached on its beak (pictures taken from
videocaptures, Reunion, C. Micheneau and J. Fournel). D, Angraecum cadetii and its raspy cricket-pollinator Glomeremus sp. with pollinaria attached on its head
(pictures taken from videocaptures with night-shot option, Reunion, C. Micheneau and J. Fournel). E, Illustration of a whole plant of A. cadetii with a visit of
the grey white-eyes (note that the bird is a simple flower visitor and does not pollinate this orchid species; pictures taken from videocaptures, Reunion, C.
Micheneau and J. Fournel).
ORCHID POLLINATION
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 1–19
7
8
C. MICHENEAU ET AL.
comparatively rich in long-tongued taxa, one species,
Panogena lingens, is by far the most common pollinator of the Madagascan angraecoid species and the sole
pollen vector of at least four orchid species (Table 1).
This hawkmoth is widely distributed in Madagascar
and shows a bimodal distribution in tongue length and
width. Two distinct morphs have been recognized, the
long- and slender-tongued morph with a mean proboscis length of c. 11–12 cm and the shorter-tongued
morph with a mean proboscis length of c. 7–8 cm. The
long-tongued morphs were often the only or most
effective pollinators (Nilsson et al., 1987; Nilsson &
Rabakonandrianina, 1988; see however, Wasserthal,
1997). In Africa, Agrius convolvuli and Coelonia fulvinotata were the two most common pollinators of
Aerangis Rchb.f. and Rangaeris (Schltr.) Summerh.
species (Fig. 2A, Martins & Johnson, 2007). On the
island of Reunion, our studies conducted on the shortspurred angraecoid orchids, Angraecum striatum and
A. bracteosum, revealed that the two white-eye species
that occur on the island, the grey white-eye, Zosterops
borbonicus, and the olive white-eye, Z. olivaceus, were
both implicated in the pollination of these orchids: grey
white-eyes are the regular pollinators of A. striatum
and occasionally pollinate A. bracteosum and olive
white-eyes are the regular pollinators of A. bracteosum, but have never been observed foraging on
A. striatum flowers (Fig. 2; Micheneau et al., 2006,
2008c). Although around 50 bird families have been
reported as flower visitors (Proctor et al. 1996), three
major avian radiations have independently evolved a
specialized nectar diet: hummingbirds (Trochilidae) in
the New World, sunbirds (Nectariniidae) in the Old
World (primarily Africa) and honeyeaters (Meliphagidae) in Australasia (e.g. van der Pijl & Dodson,
1966; Wolf, Hainsworth & Gill., 1975; Stiles, 1981;
Proctor et al., 1996; Anderson, 2003). Although these
three groups of birds have been widely reported as
orchid pollinators (e.g. van der Pijl & Dodson, 1966;
Rodríguez-Robles et al., 1992; Johnson, 1996; Singer &
Sazima, 2000; Johnson & Brown, 2004), pollination of
orchids by birds outside these three main nectarivorous groups (white-eyes in this case) was not previously known. The family Zosteropidae includes around
100 species of small arboreal songbirds (Gill, 1971;
Slikas et al., 2000). These white-eyes are known for
their high dispersal capabilities and have colonized
more oceanic islands than any other passerine family
(Moreau, 1964, cited in Gill, 1971). Although some
species of white-eyes play an important role in plant
pollination (Gill, 1971; Proctor et al. 1996; Kunitake
et al., 2004), white-eyes typically have a generalist diet
which includes fruit, insects and nectar (Gill, 1971).
More surprisingly, the third short-spurred species
of the Mascarene endemic A. section Hadrangis is
regularly pollinated at night by a medium-size ortho-
pteran species from the subtribe Gryllacridinae. This
recent discovery further constitutes the first recorded
case of regular pollination by orthopterans in extant
angiosperms (Micheneau et al., in press) and Orthoptera are mostly known as a herbivorous insect order
(see Micheneau et al., in press, for further references
on flower–orthopteran interactions).
Pollinator specificity
The observation of only a few pollinating moths per
orchid species, despite the high number of potential
pollinators observed in the vicinity of the orchids,
revealed a high degree of specialization between longspurred angraecoid orchids and their specific hawkmoth pollinators (e.g. Nilsson et al., 1987). Similarly,
it seems that each of the two bird-pollinated orchid
species is specialized for efficient pollination by only
one bird species (Micheneau et al., 2006). This was
unexpected, as bird-pollination in orchids generally
involves more than one bird pollinator. For example,
three hummingbird species have been reported pollinating Sacoila lanceolata (Aubl.) Garay (Spiranthinae
Lindl. ex Meisn., Orchidoideae Eaton) in southern
Brazil (Phaethornis eurynome, Leucochloris albicollis
and female Thalurania glaucopis) (Singer & Sazima,
2000) and, although only one hummingbird species
(Chlorostilbon maugaeus) was proposed as the
pollinator of Comparettia falcata Poepp. & Endl.
(Oncidiinae Benth., Epidendroideae) in Puerto Rico
(the only hummingbird species found in the study
area), another hummingbird (Amazilia tzacatl) was
recorded as the pollinator of this orchid in Peru
(Rodríguez-Robles et al., 1992). Satyrium carneum
(Dryand.) Sims and S. princeps Bolus (Satyriinae,
Orchidoideae) are often pollinated by two or more
sunbird species in South Africa (Nectarina spp.)
(Johnson, 1996) and, even in the unusual cases in
Disa chrysostachya Sw. and D. satyriopsis Kraenzl.
(Disinae Benth., Orchidoideae), in which sunbirds
transfer pollen with their feet from flower to flower, at
least two species of sunbirds (Nectarina famosa and
Cinnyris talatala) are involved (Johnson & Brown,
2004). The lack of records of specialization in birdpollination systems in orchids may result from the
facts that (1) many birds are generalist foragers and
(2) pollination by birds is difficult to observe because
of their furtive behaviour (van der Pijl & Dodson,
1966). Difficulties involved in making such observations mean that the incidence of orchid–bird interactions is likely to have been underestimated.
Despite the fact that the flowers of Angraecum
cadetii were frequently visited during both night and
day by a range of flower visitors (mostly birds and
nocturnal arthropods; see Micheneau et al., in press,
for further details), only raspy crickets were observed
carrying pollinaria and pollinating orchid flowers
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 1–19
ORCHID POLLINATION
(Micheneau et al., in press). This suggested that this
unexpected interaction involved a highly specialized
pollination system between the orchid and the
orthopteran.
Specialization towards a pollinator group or a
single specific pollinator is thought to maximize the
efficiency of pollination, by reducing the risk that a
generalist visitor wastes pollen in visiting foreign
flowers. Especially in orchids, in which most species
have their pollen packed in a unique structure, the
pollinarium, that is exported in its entirety at one
time by a single visitor, the loss of pollen constitutes
a massive loss of the male sex function (Tremblay,
1992; Johnson, Neal & Harder, 2005; Harder &
Johnson, 2008). However, if the reduction of the
number of pollinators enhances the efficiency of pollination, it also results in reproduction being strongly
limited by pollinators (Tremblay et al., 2005), making
orchids more dependent on their pollinators than the
reverse (Nilsson, 1992). Such asymmetrical pollination systems are common among angiosperms (Bascompte, Jordano & Olesen, 2006) and are particularly
well illustrated in the angraecoid orchids. Although
long-spurred angraecoid species are often specialized
to their specific hawkmoth pollinators (P. lingens in
particular), sphingids, in turn, are generalist foragers, opportunistically exploiting a wide variety of
orchids and other plants. Asymmetrical pollination
systems are also evident in bird–orchid interactions.
Both white-eye species are extreme generalists on
Reunion, foraging on various flowers and adding
fruits, seeds and insects to their diet. In addition, the
flowering time of Angraecum spp., during which birds
may survive on orchid nectar, is limited (i.e. approximately 1.5 months during the wet season).
POLLINATOR
BEHAVIOUR
In all study cases, the crepuscular activity of the
hawkmoths observed foraging on long-spurred flowers
was extremely limited, only taking place in the
evening between 17:15 and 19:30 h, whether the
observations were made in Africa (Luyt & Johnson,
2001; Martins & Johnson, 2007) or in Madagascar
(Nilsson et al., 1985; Nilsson & Rabakonandrianina,
1988). At the same time, most observations were
undertaken during these crepuscular hours (rarely
after 20.00 h). Local weather conditions may affect
hawkmoth foraging, which is not observed in heavy
rain or strong winds (Martins & Johnson, 2007). The
average duration of flower visits ranged from 1 to 7 s,
lasting less than 2 s in most observations. Typically,
hawkmoths, ‘smelling them in the breeze’, reached
the orchids in a ‘zigzag flight upwind’, indicating a
long-distance attraction by the strong scent emitted
by the flowers (Nilsson et al., 1987), the intensity of
9
which became stronger at dusk. At a short distance,
hawkmoths hovered in front of the flowers, easily
distinguishable by their white colour, and inserted
their unrolled proboscis into the spur, pressing their
heads towards the orchid column while collecting the
nectar. In the majority of species, pollinaria became
attached to the dorsal surface of the proboscis at a
distance from the base which varied both among
and within species, depending on the relationship
between the length of the proboscis and orchid spur,
except for Angraecum arachnites Schltr. in which
pollinaria were attached to the ventral base of the
proboscis of Panogena lingens because of the orientation of the orchid lip, and Aerangis fuscata (Rchb.f.)
Schltr. in which all pollinaria were attached to the
head of the moth (Table 1, Fig. 3). Martins & Johnson
(2007) noted that pollinaria were often attached to
the areas of the head that were worn and thus lacked
scales. A moth may carry pollinaria of different orchid
species and the number of pollinaria found on the
proboscis of a moth was also variable (Nilsson et al.,
1987; Nilsson & Rabakonandrianina, 1988). As a
maximum, Luyt & Johnson (2001) found 20 pollinaria
of Mystacidium venosum within 0.6 cm of each other
on a single proboscis of Nephele accentifera. Pollinaria
attach firmly to the pollinators by their sticky viscidia, which adhere most effectively to the smooth
surfaces of the proboscis instead of hairy zones of
their heads (in contrast to the powdery pollen of most
angiosperms). This firm fixation allows the pollinaria
to remain attached to the bodies of the pollinators for
long periods, which in turn allows the pollinators to
disperse pollen over long distances and to ensure
effective outcrossing (e.g. Nilsson et al., 1985, 1987;
Nilsson & Rabakonandrianina, 1988; Nilsson, Rabakonandrianina & Pettersson, 1992). For instance,
Wasserthal (1997) reported that a pair of undeposited
pollinia of A. sesquipedale remained undamaged on
the base of the tongue of a female Xanthopan morganii var. praedicta for almost 25 days (see also Luyt &
Johnson, 2001, for experiments on pollen longevity).
In addition to the firm adhesion, bending of pollinaria
has also been reported to occur in the majority of
long-spurred species studied. Typically, a few minutes
after the pollinarium is removed from a flower, the
stipes undergo a bending movement of 90° from their
initial position, changing the orientation of the pollinia, which become parallel to the axis of the proboscis, and correctly orient to allow pollen to be deposited
on conspecific stigmas. These bending movements
of pollinaria are assumed to preclude geitonogamy
(selfing between flowers of the same plants) (e.g.
Darwin, 1862; Wasserthal, 1997; Johnson & Edwards,
2000; Luyt & Johnson, 2001; Peter & Johnson, 2006).
White-eyes were active on flowers of Mascarene
Angraecum spp. for the whole day from 06:02 h
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 1–19
10
C. MICHENEAU ET AL.
Figure 3. Attachment distributions of pollinaria of angraecoid orchids on the proboscis of Panogena lingens. Aa,
Angraecum arachnites; Ac, Angraecum compactum; Af, Aerangis fuscata; Jt, Jumellea teretifolia; Ng, Neobathiea
grandidierana (modified from Nilsson et al., 1987).
(earliest visit recorded) to 18.05 h (latest visit
recorded), whether the weather was sunny or gloomy
and rainy (Micheneau et al., 2006, 2008c; C. Micheneau & J. Fournel, unpubl. data). The two bird
species, Z. olivaceus and Z. borbonicus, adopted the
same behaviour while feeding on orchid flowers. Typically, they landed on a leaf or inflorescence and
probed all ‘fresh-looking’ flowers within reach, moving
around the inflorescence rachis if necessary. The time
spent on orchids varied from 9 to 27 s (Micheneau
et al., 2006). To reach the nectar in the spurs, the
birds had to brush against the column and to pick up
pollinaria as they retreated from the flowers. Pollinarium attachment on the beaks contrasted strongly
between the two orchid species in relation to their
floral morphology (i.e. flower opening and spur
length). Foraging on A. striatum involved pollinarium
attachment on both the upper and lower base of the
beak (Fig. 2B), whereas pollinaria were always fixed
at the extreme tip of the beak for A. bracteosum.
Although birds may carry a large number of pollinaria, it was not rare to observe them cleaning their
beaks on tree fern stipes or nearby hardwood species
to remove their conspicuous packages.
Raspy crickets were observed foraging on flowers of
A. cadetii only during the darkest hours of night,
between 19:50 and 04:40 h. In contrast to the furtive
behaviour of both sphingids and birds, visits by these
insular orthopterans could take a long time, up to
41 s for a single flower! ‘Typically, raspy crickets
reached orchid flowers by climbing up the leaves or
jumping across from neighbouring plants. In all successful pollination events, the raspy cricket positioned
itself on the fleshy lip of the flower with its dorsal side
orientated towards the orchid column and probed
deep within the spur. Pollinaria of the orchid became
stuck to the head of the crickets as they retreated
from flowers’ (Micheneau et al., in press).
POLLINATION
AND REPRODUCTIVE SUCCESS
Compilation of data from the literature indicated that
pollination and fruiting success did not differ markedly between angraecoid orchids adapted to different
pollinator groups, although pollination efficiency
tends to be slightly higher in sphingid-pollinated
flowers than in cases of bird-pollination (Fig. 4). Fruit
set averaged approximately 17% for Madagascan–
African moth-pollinated species, 13% for Mascarene
bird-pollinated ones and 22% for Mascarene A. cadetii
pollinated by orthopterans. Whatever the pollinator
group, fruit set is however, close to the general mean
of 17% reported for tropical orchids (Tremblay et al.,
2005). Considering each pollinator group, fruit set
resulting from hawkmoth pollination ranged from 3%
for Aerangis confusa J.Stewart (Kenya, Martins and
Johnson, 2007) to 41% for Angraecum arachnites
(Madagascar, Nilsson et al. 1985) and averaged 17%.
This mean value is much lower than the average of c.
45% calculated from data found in the literature
(Tremblay et al., 2005) for tropical reward mothpollinated orchids (for comparison, fruit set reaches
approximately 51% for temperate reward mothpollinated species; Tremblay et al., 2005).
Reproductive success of bird-pollinated Angraecum
spp. (c. 13%, Table 2) is also lower than the general
median reported in the literature for bird-pollinated
orchids (54%; Tremblay et al., 2005). However, this
level of fruit set is close to the hummingbirdpollinated Comparettia falcata (c. 18%), which shares
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 1–19
ORCHID POLLINATION
11
Figure 4. Comparison of pollination and reproductive success between hawkmoth- and bird-pollinated angraecoid
orchids. Mean (± SD) of pollinaria removal, pollinaria deposition and fruit set is presented. Data were compiled from
Nilsson et al., 1985; Nilsson & Rabakonandrianina, 1988; Wasserthal, 1997; Luyt & Johnson, 2001; Martins & Johnson,
2007 for moth-pollinated species and from Micheneau et al., 2006, 2008c for bird-pollinated species.
Table 2. Summary of floral features and reproductive success according to reproductive strategy
Pollinator groups
Hawkmoths*
Birds†
Orthopterans‡
Self-pollination§
Location
Flower colour
Madagascar
White or
greenish–white
<5
4.6–33.3‡
Filiform, or spirally
twisted
Narrow
38.9 ± 57.1 (9)
15.2 ± 5.1 (12)
Strong the evening
Reunion
White
Reunion/Mauritius expected
White/cream–white
Reunion
Cream–white
>5
0.8–1.2
Conical
<5
0.6 (mean)
Conical
1
13.8 (mean)
Filiform
Large¶
6.3 ± 2.0 (2)
9.7 ± 0.1 (2)
Not detectable
Very large
14.5 ± 13.7 mL (25)
12.3 ± 3.6 (21)
Discrete (at night only)
Narrow
6.1 ± 6.1 (9)
10.7 ± 1.3 (6)
Not detectable
Dominated by
aromatics**
17.0
No volatile compound
Dominated by (E)-b-ocimene
at night
21.7
Indole at night
Flowers/inflorescence
Spur length (cm)
Spur shape
Spur opening
Nectar volume (mL)
% sugar (g/100 g)
Floral scent
(human nose)
Floral scent
composition
Fruit set (%)
12.6
62.8
Mean ± SD (N) are presented for nectar properties. N corresponds to the number of species compiled from the literature,
except for Orthopterans and self-pollination, for which N corresponds to the number of individuals sampled in the species
Angraecum cadetii and Jumellea stenophylla, respectively. If variation were observed in nectar sugar concentration for
a species, the highest value was chosen.
*Compiled data from Nilsson et al. (1985, 1987); Nilsson & Rabakonandrianina (1988); Wasserthal (1997); Luyt & Johnson
(2001); Martins & Johnson (2007) (study species are Angraecum arachnites, A. compactum Schltr., A. sororium,
A. sesquipedale, Aerangis articulata (Rchb.f.) Schltr., A. brachycarpa (A.Rich.) Durand & Schinz, A. confusa, A. ellisii,
A. fuscata, A. kotchyana, A. thomsonii, Jumellea teretifolia Schltr., Mystacidium venosum, Neobathiea grandidierana
(Rchb.f.) Garay and Rangaeris amaniensis (Kraenzl.) Summerh).
†Compiled data from Micheneau et al. (2006; 2008c) (study species are Angraecum bracteosum and A. striatum).
‡Data from Micheneau et al. (in press) (study species is Angraecum cadetii).
§Data from Micheneau et al. (2008b) (study species is Jumellea stenophylla).
¶Angraecum bracteosum display a callus on the lip, which restricted flower’s entrance.
**Kaiser (1993).
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 1–19
12
C. MICHENEAU ET AL.
both an epiphytic habit and a tropical distribution
(Rodríguez-Robles et al., 1992) with these Angraecum
spp.
Surprisingly, flower visits by orthopterans involved
a high rate of fruiting success, averaging 22% at the
study site of the Plaine des Palmistes in Reunion
(average for 3 years). This rate is much higher than
the 10% fruit set recorded for the bird pollinated
sister species at the same study site and in the same
years (Micheneau, 2005; Micheneau et al., 2008c).
Reproductive success seems to be generally
pollinator-limited in the angraecoid orchids (e.g.
Wasserthal, 1997; Luyt & Johnson, 2001; Micheneau,
2005; Micheneau et al., 2006, 2008c). However,
the spectacular rate of flower abortion found in
Angraecum striatum (Micheneau et al., 2006) and the
low rate of fruit set in Aerangis ellisii (Rchb.f.) Schltr.
in spite of a high frequency of both pollen removal
and deposition (Nilsson & Rabakonandrianina, 1988)
suggest that in some species resource allocation may
also affect reproductive success.
FLOWER
MORPHOLOGIES AND REPRODUCTIVE
STRATEGIES
Hawkmoth-pollinated flowers
Long-spurred angraecoid orchids show a clear suite of
floral adaptations to hawkmoth pollination, including
floral traits involved in pollinator attraction (i.e.
white flower and strong scent), pollinator fidelity
(large sugar-rich nectar reward, situated in deep
spurs easily accessible for long-tongued moths) and
structural modifications to the column, the lip and/or
the spur which all contribute to favourable contact
between the head or proboscis of the moth and the
orchid column and thus result in efficient pollinarium
removal or deposition. The fact that in most species
the lip lacks a landing platform is thought to facilitate
pollination by hawkmoths, as they are able to probe
nectar while hovering above the flowers without
requiring any support from the flower (Luyt &
Johnson, 2001). However, a landing platform may
exist in some species, such as the very long-spurred
Angraecum sesquipedale and A. sororium. Especially
for these two species, the landing platform is thought
to facilitate pollination by hawkmoths that swing–
hover such as Xanthopan morganii praedicta and
Coelonia solani (Wasserthal, 1997). In addition, particular shapes of lips may further function as a
mechanical guide to orient the base of the proboscis
into the spur (Nilsson et al., 1985; Luyt & Johnson,
2001). Specific adaptations of the rostellum may also
extend over the mouth of the spur, flanking the
entrance of the spur, presumably forcing the head of
the pollinator into close contact with the orchid
column (e.g. Aerangis elisii, Nilsson & Rabakonandri-
anina, 1988; see also Wasserthal, 1997). Nectar production in the spur is another factor that has been
viewed as being of crucial importance for successful
pollination by hawkmoths (e.g. Darwin, 1862; Nilsson
et al., 1985). In most flowers, the nectar is located
only at the base of the spur, forcing the pollinator to
probe deep into the spur to reach the nectar or ‘to
drain the last drop’ (Darwin, 1862), so that its head
makes the best contact with the orchid column to
ensure successful pollen export and import (e.g.
Darwin, 1862; Nilsson et al., 1985, 1987; Nilsson &
Rabakonandrianina, 1988; Wasserthal, 1997; Martins
& Johnson, 2007). In addition, spirally twisted spurs
found in Aerangis thomsonii (Rolfe) Schltr., A.
kotschyana (Rchb.f.) Schltr. and Angraecum arachnites may also serve identical purposes. Spirally
twisted spurs involve tight frictions between orchid
spur and hawkmoth tongue during nectar consumption, which may encourage moths to probe deeper into
the spur and to stay longer in close contact with the
reproductive organs of the orchid.
Bird-pollinated flowers
Although they are phylogenetically close to Malagasy
species that perfectly match the sphingophilous pollination syndrome (Micheneau et al., 2008a), the Mascarene bird-pollinated Angraecum spp. show the
usual convergent adaptations observed in other birdpollinated orchids. Except for the colour of the flower,
which is pure white rather than vividly coloured as
in typical bird-pollinated flowers, A. striatum and
A. bracteosum display multi-flowered inflorescences
of unscented and short-spurred flowers, which are
rather fleshy in texture. In addition, A. bracteosum
flowers have a strong fold (callus) on the lip, restricting the opening of the flower. This callus is a convergent feature often found in bird-pollinated orchids
and may force the birds to push their beaks against
the orchid column to reach the nectar in the spur (e.g.
van der Pijl & Dodson, 1966; van der Cingel, 2001).
Orthopteran-pollinated flowers
Flower morphology of A. cadetii appears to be the
result of a suite of floral adaptations for efficient
pollination by raspy crickets (Micheneau et al., in
press). Sepals and petals are quite small and fleshy;
no damage was observed on these flower parts, suggesting that orthopterans do not usually predate the
orchids (Micheneau et al., in press). The shape and
the size of the pollinia (quite large, flat and triangular), are also atypical for the genus Angraecum, especially if compared with the small ball-like pollinia of
the bird-pollinated species of A. section Hadrangis
(Fig. 5). In addition, there is a close match in size
between the head of the insect and the nectar-spur
opening (Micheneau et al., in press; S. Hugel, unpubl.
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 1–19
ORCHID POLLINATION
13
Figure 5. Comparison of the shape and the size of pollinia between bird- and orthopteran-pollinated species within
Angraecum section Hadrangis. A, Orthopteran-pollinated A. cadetii. B, Bird-pollinated A. bracteosum.
data). Finally, the floral bouquet of A. cadetii (i.e.
nocturnal emission of monoterpene-dominated scent;
Micheneau et al., in press) probably plays a major role
in attracting raspy crickets, which use their long
antennae to explore their surroundings at night (C.
Micheneau, pers. observ.; S. Hugel, pers. comm.).
Self-pollinating flowers
The study of different floral traits related to plant–
pollinator interactions, namely flower longevity, spur
length, nectar properties and scent production, have
been investigated in the autogamous long-spurred
Jumellea stenophylla (Frapp. ex Cordem.) Schltr.,
which is endemic to Reunion (Micheneau et al.,
2008b). Results have shown that flower longevity of
this self-pollinating species was much shorter (only
4–5 days) than that of hawkmoth-pollinated orchids
(c. 25 days, Luyt & Johnson, 2001). This short
flower lifetime was associated with autonomous
self-pollinations that activated flower senescence.
Although spur length of J. stenophylla (c. 13.8 cm) is
within the reported spur size of long-spurred angraecoid orchids studied, the species only produces a relatively small amount of nectar (c. 6.1 mL) and flowers
do not emit a strong and sweet scent at dusk (see
Micheneau et al., 2008b for further details) This lack
of floral scent, associated with the high degree of
auto-pollinated flowers with a short lifespan, makes
the flowers highly unattractive for pollinators and
consequently precludes any chance of this orchid
being cross-pollinated.
EVOLUTION
OF POLLINATOR-LINKED FLORAL TRAITS
Nectar properties
Nectar volume and sugar concentration in angraecoid
orchids show clear patterns in relation to pollinator
group. In hawkmoth-pollinated species, nectar sugar
concentration averages 15.2%, whereas it is only 9.7%
in bird-pollinated flowers (Table 2). The values for
hawkmoth-pollinated angraecoid orchids are similar
to those found in hawkmoth-pollinated plants more
generally (Pyke & Waser 1981) and the dilute nectar
found in angraecoid orchids conforms almost exactly
to the pattern observed for other plants pollinated by
short-billed opportunistic birds (Johnson & Nicolson,
2008). Plants pollinated by specialist flower feeding
birds (hummingbirds and sunbirds) tend to produce
nectar with a sugar concentration around 20%,
whereas those pollinated by short-billed opportunistic
birds tend to produce nectar with much lower concentrations around 10% (Johnson & Nicolson, 2008).
Gradients in nectar sugar concentrations along the
length of the nectar column were recently reported to
occur within spurs in African Aerangis and Rangaeris
spp. (Martins & Johnson, 2007). In all study species,
nectar was significantly more diluted towards the
mouth of the spur than at the tip (concentrations
ranged from c. 1% at the proximal end of the spur to
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14
C. MICHENEAU ET AL.
c. 20% at the distal end). Nectar sugar gradients may
have the same function as spirally twisted spurs and
the presence of the nectar only in the lower part of the
lip, i.e. they encourage the moth to go as deep as
possible into the spur while probing nectar, enhancing
at the same time the chance to ensure efficient pollination (Martins & Johnson, 2007). Post-pollination
reabsorption of sugars from spurs has also been
reported for two aerangoid orchid species (Koopowitz
& Marchant, 1998; Luyt & Johnson, 2002) and this
may mobilize resources for fruit development
(Koopowitz & Marchant, 1998; Luyt & Johnson,
2002).
The sugar composition of nectar of only one angraecoid species has been investigated so far (Mystacidium venosum, Luyt & Johnson, 2001). The nectar
of this hawkmoth-pollinated orchid proved to be especially sucrose-rich (87% sucrose, 10% fructose and 3%
glucose). It would be worthwhile in future research to
develop further these comparative studies of nectar
sugar composition, with the aim of investigating evolutionary patterns of this floral trait between birdand moth-pollinated species within the angraecoid
orchid group (Johnson & Nicolson, 2008). In particular, one could then test the prediction that there
should be an association between opportunistic bird
pollinators and hexose-dominated nectar, based on
the inability of these birds to digest simple sugars
(e.g. Martínez del Rio, Baker & Baker, 1992).
Long nectar spur evolution
Darwin’s seminal work on the angraecoid orchid
Angraecum sesquipedale triggered the beginning of a
long debate about the evolution of long floral spurs.
The two competing explanations for these traits are
the Darwinian ‘coevolutionary race’ model (1862) and
the ‘pollinator shift’ model developed by Stebbins
(1970). The Darwinian ‘coevolutionary race’ model
attributes adaptive elongation of the tongues of the
moths and the spurs of the flowers to reciprocal
coevolution, as a result of a gradual increase as a
result of mutual benefit (gain in reproduction efficiency for the orchid and gain in nectar foraging
efficiency for the hawkmoth). The alternative ‘pollinator shift’ model states that long tongues in hawkmoths were present before the long spurs of the
orchids and evolved without any reciprocal interactions with them (Wasserthal, 1997; Whittall &
Hodges, 2007). This model attributes the evolution of
long nectar spurs to punctuated shifts to successive
pollinators with longer tongues. Both models agree,
however, with Darwin’s idea that longer spurs
evolved under directionally selective pressure exerted
by long-tongued pollinators. Darwin did not exclude
the possibility that longer tongues in hawkmoth may
have evolved from selection on body size ‘in relation to
their conditions of life, either in the larval or mature
state’ (Darwin, 1862) or in response to the spur length
of other plants. Much more controversial has been
Wasserthal’s (1997) assertion that the evolution of
long tongues in hawkmoths was driven by selection
imposed by flower predators, rather than availability
of nectar in deep tubular flowers (e.g. Wasserthal,
1997; Nilsson, 1998a, b; Svensson, Rydell & Töve,
1998; Wasserthal, 1998).
Because the interactions between angraecoid
orchids and hawkmoths are mostly asymmetric
(Nilsson & Rabakonandrianina, 1988), it seems likely
that coevolution was diffuse at the guild level and not
strictly pairwise. It also seems likely that many
members of these guilds became adapted to longtongued hawkmoths via a pollinator shift rather than
through coevolution. However, the relationships
between long-spurred angraecoid orchids and their
hawkmoth pollinators remain largely unknown if we
consider the small number of species that has been
studied (< 20 species) against the number of existing
species (> 760 species in Angraecinae s.l., i.e. including Aerangidinae). We need to expand our knowledge
to better assess the evolutionary outcomes between
these orchids and their pollinators. In particular, finescale studies of geographical variation in mutualistic
traits such as tongue length and nectar depth may
reveal co-evolutionary processes at the population
level (see Anderson & Johnson, 2008). However, much
of the evolutionary potential of these orchids and
their pollinators may already have been lost as a
result of the massive destruction of primary forests in
Madagascar and the large number of fragmented
populations (i.e. reduction in population size and
genetic diversity can have a severe effect on the
evolutionary potential, e.g. Hubbell et al., 2008).
CONCLUDING REMARKS
Orchids should be studied more because they epitomize evolution in its most dynamic aspect, the rapid production of an
incredibly diverse array of species (Chase et al., 2003).
Orchids have been a model system for studying floral
adaptation and diversification ever since Darwin’s
influential book on the subject was published in 1862.
They provide some of the most exceptional examples of
highly specialized interactions between animals and
plants. Not surprisingly, orchid pollination has been
intensively studied relative to that in other extant
angiosperms, with entire books dedicated to the
subject (e.g. Darwin, 1862, 1877; van der Pijl &
Dodson, 1966, van der Cingel, 1995, 2001), book chapters (e.g. Proctor et al. 1996, Roberts, 2003; see also
Dressler, 1981, 1993) and numerous high-impact publications (e.g. Nilsson, 1983b, 1992; Romero & Nelson,
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 1–19
ORCHID POLLINATION
1986; Nilsson et al., 1992; Johnson & Nilsson, 1999;
Schiestl et al., 1999, 2003; Cozzolino & Widmer, 2005;
Liu et al., 2006; Ramírez et al., 2007).
The unique, unexpected and diverse orchid pollination systems provide excellent opportunities for determining how pollinator-mediated selection has shaped
the evolution of floral traits (e.g. flower scent, colour
and spur length) and how shifts between pollinators
may be responsible for patterns of macroevolution at
the species level and above. However, in spite of the
large size of this model family and the long history of
orchid pollination biology, the identity and specificity
of most orchid pollinators are unknown and remain
inadequately studied, especially in the tropics where
the family has undergone extensive diversification.
Finally, highly specialized pollination interactions,
such as those exemplified by orchids, are highly vulnerable to changes in populations and habitats. As
Darwin pointed out while the pollinating sphingid of
A. sesquipedale was still undiscovered: ‘If such great
moths were to become extinct in Madagascar, assuredly the Angræcum would become extinct’ (Darwin,
1862). Once again, Darwin led the way in drawing
this important connection between evolutionary
studies and the ‘real-world’ problem of conservation.
This is especially relevant today because of the
present context of pollinator decline (Buchmann
& Nabham, 1996; Kearns, Inouye & Waser, 1998;
Biesmeijer et al., 2006; Ghazoul, 2006) as a result of
habitat loss (Harris & Johnson, 2004; Aguilar et al.,
2006) and climate change (Deutsch et al., 2008).
ACKNOWLEDGEMENTS
We warmly thank T. Pailler and J. Fournel (University of La Réunion) for their contributions to research
involved in pollination biology of Mascarene angraecoid orchids.
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